The Association of Nocturnal Seizures and Interictal Cardiac/Central Autonomic Function in Frontal Lobe Epilepsy: Heart Rate Variability and Central Autonomic Network Analysis

Woojun Kim,1 Hyunjo Lee,2 Kyung Won Lee,3 Eunjin Yang,3 Seonghoon Kim3 1Department of Neurology, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea; 2Department of Neurology, Ulsan University Hospital, College of Medicine, University of Ulsan,...

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Main Authors: Kim W, Lee H, Lee KW, Yang E, Kim S
Format: Article
Language:English
Published: Dove Medical Press 2023-10-01
Series:Neuropsychiatric Disease and Treatment
Subjects:
Online Access:https://www.dovepress.com/the-association-of-nocturnal-seizures-and-interictal-cardiaccentral-au-peer-reviewed-fulltext-article-NDT
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author Kim W
Lee H
Lee KW
Yang E
Kim S
author_facet Kim W
Lee H
Lee KW
Yang E
Kim S
author_sort Kim W
collection DOAJ
description Woojun Kim,1 Hyunjo Lee,2 Kyung Won Lee,3 Eunjin Yang,3 Seonghoon Kim3 1Department of Neurology, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea; 2Department of Neurology, Ulsan University Hospital, College of Medicine, University of Ulsan, Ulsan, Republic of Korea; 3Department of Neurology, Uijeongbu St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of KoreaCorrespondence: Seonghoon Kim, Department of Neurology, The Catholic University of Korea, College of Medicine, Uijeongbu St. Mary’s Hospital, 271 Cheonbo-ro, Uijeongbu-si, Gyeonggi-do, Seoul, Republic of Korea, Tel +82-31-820-3114, Fax +82-31-821-3661, Email antilefty4@gmail.comPurpose: Patients with epilepsy frequently experience autonomic dysfunction, closely related to sudden unexplained death in epilepsy (SUDEP). SUDEP occurs most often at night or during sleep, and frequent nocturnal seizures are an established risk factor. This study investigated the influence of nocturnal seizures on autonomic dysfunction in epilepsy.Patients and Methods: This retrospective study enrolled frontal lobe epilepsy (FLE) patients who performed 24-hour EEG monitoring. All participants were divided into nocturnal FLE (NFLE, > 90% of seizures occurring during sleep) or diurnal FLE (DFLE) groups. EEG and ECG signals were simultaneously obtained during waking and sleep stages. EEG current density source and connectivity analysis of the autonomic network were performed. ECG was analyzed across time and frequency domains heart rate variability (HRV) analysis method was used. The obtained parameters were compared between the NFLE and DFLE groups.Results: Fifteen NFLE and 16 DFLE patients were enrolled with no significant difference in age, sex, disease duration, seizure frequency, or the number of anti-seizure medications between the two groups. During sleep, a decrease in HRV parameters and an increase of the beta-1 (13– 22 Hz) current source density power in the bilateral paracentral lobule (BA4,5,6), precuneus (BA7), and cingulate (BA31) were observed in the NFLE group compared to DFLE group. The NFLE group also showed hyperconnectivity in the central autonomic (12 edges distributed over 10 nodes), sympathetic (2 edges distributed over 3 nodes), and parasympathetic (4 edges distributed over 6 nodes) beta-1 frequency band networks during sleep. During wakefulness, central and cardiac autonomic variables were not significantly different between the NFLE and DFLE groups.Conclusion: Interictal cardiac and central autonomic dysfunction occurred simultaneously and can be attributed to the brain-heart autonomic axis. Our findings suggest that nocturnal seizures may contribute to interictal autonomic dysfunction during sleep in people with epilepsy.Keywords: nocturnal seizure, heart rate variability, central autonomic network, sleep, autonomic dysfunction
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spelling doaj.art-e24c4135c7094e549529e09ecf93317c2023-10-17T02:42:29ZengDove Medical PressNeuropsychiatric Disease and Treatment1178-20212023-10-01Volume 192081209187128The Association of Nocturnal Seizures and Interictal Cardiac/Central Autonomic Function in Frontal Lobe Epilepsy: Heart Rate Variability and Central Autonomic Network AnalysisKim WLee HLee KWYang EKim SWoojun Kim,1 Hyunjo Lee,2 Kyung Won Lee,3 Eunjin Yang,3 Seonghoon Kim3 1Department of Neurology, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea; 2Department of Neurology, Ulsan University Hospital, College of Medicine, University of Ulsan, Ulsan, Republic of Korea; 3Department of Neurology, Uijeongbu St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Republic of KoreaCorrespondence: Seonghoon Kim, Department of Neurology, The Catholic University of Korea, College of Medicine, Uijeongbu St. Mary’s Hospital, 271 Cheonbo-ro, Uijeongbu-si, Gyeonggi-do, Seoul, Republic of Korea, Tel +82-31-820-3114, Fax +82-31-821-3661, Email antilefty4@gmail.comPurpose: Patients with epilepsy frequently experience autonomic dysfunction, closely related to sudden unexplained death in epilepsy (SUDEP). SUDEP occurs most often at night or during sleep, and frequent nocturnal seizures are an established risk factor. This study investigated the influence of nocturnal seizures on autonomic dysfunction in epilepsy.Patients and Methods: This retrospective study enrolled frontal lobe epilepsy (FLE) patients who performed 24-hour EEG monitoring. All participants were divided into nocturnal FLE (NFLE, > 90% of seizures occurring during sleep) or diurnal FLE (DFLE) groups. EEG and ECG signals were simultaneously obtained during waking and sleep stages. EEG current density source and connectivity analysis of the autonomic network were performed. ECG was analyzed across time and frequency domains heart rate variability (HRV) analysis method was used. The obtained parameters were compared between the NFLE and DFLE groups.Results: Fifteen NFLE and 16 DFLE patients were enrolled with no significant difference in age, sex, disease duration, seizure frequency, or the number of anti-seizure medications between the two groups. During sleep, a decrease in HRV parameters and an increase of the beta-1 (13– 22 Hz) current source density power in the bilateral paracentral lobule (BA4,5,6), precuneus (BA7), and cingulate (BA31) were observed in the NFLE group compared to DFLE group. The NFLE group also showed hyperconnectivity in the central autonomic (12 edges distributed over 10 nodes), sympathetic (2 edges distributed over 3 nodes), and parasympathetic (4 edges distributed over 6 nodes) beta-1 frequency band networks during sleep. During wakefulness, central and cardiac autonomic variables were not significantly different between the NFLE and DFLE groups.Conclusion: Interictal cardiac and central autonomic dysfunction occurred simultaneously and can be attributed to the brain-heart autonomic axis. Our findings suggest that nocturnal seizures may contribute to interictal autonomic dysfunction during sleep in people with epilepsy.Keywords: nocturnal seizure, heart rate variability, central autonomic network, sleep, autonomic dysfunctionhttps://www.dovepress.com/the-association-of-nocturnal-seizures-and-interictal-cardiaccentral-au-peer-reviewed-fulltext-article-NDTnocturnal seizureheart rate variabilitycentral autonomic networksleepautonomic dysfunction
spellingShingle Kim W
Lee H
Lee KW
Yang E
Kim S
The Association of Nocturnal Seizures and Interictal Cardiac/Central Autonomic Function in Frontal Lobe Epilepsy: Heart Rate Variability and Central Autonomic Network Analysis
Neuropsychiatric Disease and Treatment
nocturnal seizure
heart rate variability
central autonomic network
sleep
autonomic dysfunction
title The Association of Nocturnal Seizures and Interictal Cardiac/Central Autonomic Function in Frontal Lobe Epilepsy: Heart Rate Variability and Central Autonomic Network Analysis
title_full The Association of Nocturnal Seizures and Interictal Cardiac/Central Autonomic Function in Frontal Lobe Epilepsy: Heart Rate Variability and Central Autonomic Network Analysis
title_fullStr The Association of Nocturnal Seizures and Interictal Cardiac/Central Autonomic Function in Frontal Lobe Epilepsy: Heart Rate Variability and Central Autonomic Network Analysis
title_full_unstemmed The Association of Nocturnal Seizures and Interictal Cardiac/Central Autonomic Function in Frontal Lobe Epilepsy: Heart Rate Variability and Central Autonomic Network Analysis
title_short The Association of Nocturnal Seizures and Interictal Cardiac/Central Autonomic Function in Frontal Lobe Epilepsy: Heart Rate Variability and Central Autonomic Network Analysis
title_sort association of nocturnal seizures and interictal cardiac central autonomic function in frontal lobe epilepsy heart rate variability and central autonomic network analysis
topic nocturnal seizure
heart rate variability
central autonomic network
sleep
autonomic dysfunction
url https://www.dovepress.com/the-association-of-nocturnal-seizures-and-interictal-cardiaccentral-au-peer-reviewed-fulltext-article-NDT
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